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Neurology India
Medknow Publications on behalf of the Neurological Society of India
ISSN: 0028-3886 EISSN: 1998-4022
Vol. 58, Num. 6, 2010, pp. 886-890

Neurology India, Vol. 58, No. 6, November-December, 2010, pp. 886-890

Topic of the Issue: Original Article

Appliance of preoperative diffusion tensor imaging and fiber tractography in patients with brainstem lesions

ZhiKai Cao, JianPing Lv, Xinhua Wei, Wei Quan

Department of Neurosurgery, Guangzhou First Municipal People's Hospital Affiliated to Guangzhou Medical College, 1 Panhu Road, Guangzhou 510180, People's Republic of China
Correspondence Address: JianPing Lv, Department of Neurosurgery, Guangzhou First Municipal People's Hospital Affiliated to Guangzhou Medical College, Guangzhou - 510 080 , People's Republic of China, ljpwhx@163.com

Date of Acceptance: 10-Jul-2010

Code Number: ni10253

PMID: 21150055
DOI: 10.4103/0028-3886.73736

Abstract

Background: Surgical resection of brainstem lesions has a high risk of morbidity, because vital fasciculi in the brainstem can be damaged along the entry routes. Diffusion tensor imaging (DTI) is an in vivo method for mapping white matter fiber tracts in the brain.

Objective: To summarize the experience of surgical treatment of brainstem lesions with the assistance of DTI and fiber tractography.

Materials and Methods: A retrospective analysis clinical data of nine patients with brainstem lesions were investigated between July 2007 and September 2009. The analysis included age distribution, clinical presentation, pre- and postoperative modified Rankin score (mRS), and surgical approach. DTI and fiber tractography were used to reconstruct the corticospinal tracts and the medial lemnisci.

Results: DTI and fiber tractography showed that most of the corticospinal tracts were compressed anteriorly or anterolaterally, except for one case (posteriorly). All the medial lemnisci were displaced posteriorly or posterolaterally. Individualized surgical approaches were designed according to the information provided by DTI and fiber tractography. Total resection was achieved in two patients with brainstem cavernomas and two patients with pilocytic astrocytoma. Partial resection was performed in the other patients. The neurological functional status was better than preoperative period in eight patients, one patient with medulla oblongata astrocytoma deteriorated. The preoperative average mRS score was 2.22 points. At the time of the last follow-up, the average postoperative score had improved by 0.56 to 1.66 points.

Conclusions: DTI and fiber tractography can provide valuable information regarding the relationship between the principal fiber tracts and brainstem lesions, which is useful in neurosurgical planning.

Keywords: Brainstem, diffusion tensor imaging, lesion, surgery

Introduction

Brainstem lesions are always worrisome for the neurosurgeon, for access to brainstem is a hazardous and challenging work, carrying the risk of aggravating the neurological deficits of the patient. [1],[2] The surgical approach must be carefully designed to identify the most accessible route and minimize the damage to vital fasciculi in the brainstem. [3],[4],[5] Any method that can provide more anatomical information or enhance the safety of surgical resection will be welcome. Among magnetic resonance imaging (MRI) techniques, diffusion tensor imaging (DTI) is a procedure that measures directional diffusivity of water molecules, which is the only noninvasive in vivo method for mapping white matter fiber tracts in the human brain. [6],[7] In this study, we describe the clinical experience with nine surgically treated brainstem lesions in which DTI and fiber tractography were applied in guiding neurosurgical planning.

Materials and Methods

Patients and clinical characteristics

A retrospective analysis clinical data of nine patients with brainstem lesions were investigated between July 2007 and September 2009. All patients underwent surgical intervention with the assistance of DTI and fiber tractography in our department. There were five men and four women; age ranged from 4 to 49 years (mean, 30.1 years). The clinical presentations in all patients included hemiparesis, hemianesthesia, ataxia, vertigo, and so on. The patient's preoperative and postoperative neurological state was classified according to the modified Rankin scale (mRS) to achieve a grading of functional disturbances of daily life activities. [8] Long-term follow-up included a complete neurological examination of all patients and MRI studies. The mean follow-up period was 12 months (range, 1-24 months). The study received the approval of the ethic committee of Guangzhou medical college, and informed consent was taken from all of the participants.

Radiological examination

The scans were performed at 3 T using a Philips ACHIEVA R1 magnet (Best, The Netherlands) and an eight-channel sensitivity-encoding head coil. A single-shot spin-echo echo-planar DTI sequence was used with the following parameters: TR/TE, 4600/90; flip angle, 90°; field of view, 140 mm; matrix size, 128Χ128; number of signals averaged, 3. Diffusion sensitizing gradients were applied in 32 directions. Two b values were used: 0 and 1000 s/mm 2 . The data were obtained from 35 axial slices of 4-mm thickness with no gap. Tractography was performed on-site using the diffusion tensor tractography software (PRIDE, Philips Medical Systems) in Guangzhou first municipal people's hospital affilated to Guangzhou medical college.

Conventional MRI evaluation revealed six lesions located in the pons, two lesions in the medulla oblongata and one lesion extending from the midbrain to the pons. The lesion sizes obtained by measuring the greatest diameter in any single plane on preoperative MRI scans ranged from 1.4 to 4.2 cm (mean, 3.2 cm). To determine the anatomical relationship between the brainstem lesion and the adjacent eloquent fiber tracts, DTI color fractional anisotropy (FA) map and fiber tractography were performed. The color FA maps show the direction of white matter tracts; commissural tracts are depicted in red, association fibers such as the superior longitudinal fasciculus are displayed in green, and the superoinferiorly running projection fibers are seen in blue. In the present study, fiber tractography was used to reconstruct the corticospinal tracts and the medial lemnisci.

Surgical management

A midline suboccipital approach without vermian split was most commonly preferred (n = 7), followed by a suboccipital retromastoid approach (n = 1) and a supracerebellar infratentorial approach (n = 1). In all the patients, a thin layer of brainstem parenchyma covered the surface. Incision over the parenchyma was given over the thinnest part, away from the corticospinal tracts and the medial lemnisci if any. A radical resection was attempted in all patients. A thin layer of tumor tissue adjacent to the eloquent fiber tracts was left, if it appeared not separable from the surrounding important structure.

Results

Individualized surgical approaches were designed according to the information provided by DTI and conventional MRI. In most conditions, surgical approaches could be decided by conventional MRI (n = 8). However, the information provided by conventional MRI seemed to be not enough for the case discussed below. DTI and fiber tractography were proved to be especially valuable. The patient was a 49-year-old man presenting with acute onset of headache associated with a right hemiparesis, gait disturbance, and lower cranial nerve disturbances. Eventually he was admitted for surgery (mRS score 4). The conventional MRI showed a large cavernoma located in the pons [Figure - 1], which provided the following two available surgical approaches: a midline suboccipital approach and a retromastoidal approach. The subsequent DTI and fiber tractography confirmed that the corticospinal tracts and the medial lemnisci were compressed posteriorly because of the lesion [Figure - 2]. Therefore, we selected a suboccipital retromastoid approach. As a result, the lesion was completely resected without destroying the corticospinal tracts and the medial lemnisci [Figure - 3]. Postoperative MRI confirmed complete resection of the lesion [Figure - 1]. One year after surgery the neurological examination showed a residual mild hemiparesis, but the patient was able to walk independently and disturbances of the lower cranial nerves had resolved completely (mRS score 2).

With the assistance of the information provided by DTI and fiber tractography, we knew the relationship between the lesion and important fiber tracts. Most of the corticospinal tracts were compressed anteriorly or anterolaterally [Figure - 4], except for one case (posteriorly). All the medial lemnisci were displaced posteriorly or posterolaterally. The operating procedure became very cautious and conservative when handling tumor tissue adhesive to important white matter fiber tracts. In this study, total resection was achieved in two patients with brainstem cavernomas and two patients with pilocytic astrocytoma. Partial resection was performed in other patients who received radiotherapy one month later. There were no surgery-related deaths. Postoperatively, one patient with medulla oblongata astrocytoma underwent mechanical ventilation for a week. One month after the surgery, the neurological functional status was better than preoperative period in eight patients, whereas the patient with medulla oblongata astrocytoma deteriorated. The preoperative average Rankin score was 2.22 points. At the time of the last follow-up, the average postoperative score had improved by 0.56 to 1.66 points. A summary is given in [Table - 1].

Discussion

Because too many vital nuclei and fasciculi are densely packed in the brainstem, surgical resection of brainstem lesions remains one of the most challenging works for neurosurgeons. [2],[9],[10],[11] Many neurological deficits following surgery are caused by the injury of eloquent white matter tracts. [1],[2],[3],[12],[13] The postoperative motor or sensory function was presumably related to the integration of eloquent fiber tracts. Therefore, knowing the relationship between the lesions and the important fiber tracts is valuable for planning appropriate neurosurgical approaches. Until now, most neurosurgeons choose the neurosurgical approach almost entirely based on the location of the brainstem lesion and its proximity to the ventricle or pial surface, [1],[3],[11],[14],[15] which do not consider the anatomical relationship between the lesions and the eloquent fiber tracts. Theoretically, the lesions can arise from any region of the brainstem. Thus, the eloquent fiber tracts could be compressed in any direction. If the eloquent white matter tracts happen to locate in the route of access, the dissection would have a potential risk of destroying important fiber tracts.

For the time being, DTI is the only imaging method that can visualize the white matter tracts in the human brain in vivo. [6],[7],[16],[17],[18],[19] In modern clinical practice, one of the most important indications of DTI is to study the relationship between the principal white matter tracts and the intracerebral lesions, [20],[21] which is not available on conventional MRI. White matter involvement by a tumor can be arranged into various categories with DTI, such as displaced, invaded, edematous, and destroyed fiber tracts. Such information is extremely valuable for guiding the surgical approach and for identifying the extent of resection. Dukatz et al.[22]investigated brainstem cavernomas with DTI and fibertracking in order to calculate the anisotropy maps and to evaluate white matter trajectories pre- and postoperatively. He thought such investigation might have an impact in planning of microsurgical approaches to this surgically difficult target area. Chen et al. [23],[24] have recently reported the implementation of fibertracking into neuronavigation system during a brainstem cavernoma surgery. They considered that fibertracking was especially useful in neurosurgical planning for deep-seated brainstem lesions.

In case discussed above, the lesion was located in the lateral part of the pons. According to traditional experience, two surgical approaches (a midline suboccipital approach and a retromastoidal approach) were suitable for this situation. From previous reports, [25],[26],[27],[28] a midline suboccipital approach with or without vermian split (cerebellomedullary fissure approach) was the most frequent one, which seemed to be an appropriate approach for this patient. However, on DTI and fiber tractography, the lesion displaced both the left corticospinal tract and medial lemniscus posteriorly. Especially the 3D reconstructed image showed the corticospinal tract which seemed to be compressed posteriorly as thin as a piece of paper. So, a midline suboccipital approach would inevitably encounter the left corticospinal tract and medial lemniscus, which might lead to postoperative severe complications. Therefore, a retromastoidal approach through the lateral side of the pons was adopted and the postoperative course was favorable. [26]

We suggest that the optimal neurosurgical planning should be decided not only by the location of the lesion, but also by the relation of a lesion to the adjacent important white matter tracts, especially to the corticospinal tract and medial lemniscus. With the assistance of DTI, the surgical approach can be individualized for each patient. [23],[24] Furthermore, DTI can provide a 'safe corridor' on the brainstem and remind neurosurgeons of cautiously handling tumor tissue adhesive to the area containing important fiber tracts, which could help to improve neurosurgeons' confidence during the operation. Therefore, we strongly propose that DTI and fiber tractography should become a routine preoperative examination for brainstem lesions.

In summary, although our observation is limited, it suggests that DTI and fiber tractography could provide extremely valuable information regarding the relationship between the principal fiber tracts and brainstem lesions, which is especially useful in neurosurgical planning.

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